SENSORY ORGANS IN THE HAIRY GIRDLES OF SOME MOPALIID CHITONS

By: Esther M. Leise

Leise, E.M. (1988) Sensory organs in the hairy girdles of some mopaliid chitons. American Malacological

Bulletin 6(1):141-151.

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Abstract:

The polyplacophoran mantle secretes the shell plates, houses the gills in the pallial grooves, and forms a

muscular perinotum or girdle that encircles the shell and viscera. The epidermis of this girdle occurs as papillae

of columnar cells dispersed over an otherwise cuboidal epithelium. Depending upon the species, these papillae

can produce a variety of hard structures: calcareous scales, spicules, or spines and/or chitinous hairs. Some

papillae also produce bulbous outgrowths called nodules or "morgensternförmigen Körper" (morning star-

shaped bodies). These nodules contain the dendrites of sensory neurons and are thought to be

mechanoreceptive. Nodules can occur alone in the cuticle or in conjunction with calcareous spicules. Nodules

of this type are present in the hairs of chitons in the genus Mopalia. Hairs from other mopaliid genera are also

innervated, although they can lack these particular structures. In most species of chitons that I examined,

nodules are made in conjunction with the ventral girdle spicules and the marginal spicules. These presumptive

mechanoreceptors could be ubiquitous among chitons, as all species possess marginal spicules and overlapping

ventral spicules. Hairs could have evolved to extend the reach of these tactile receptors beyond the surface of

the animal's body, as well as to provide mechanical protection from desiccation and predation.

Article:

The external surfaces of the polyplacophoran girdle are armed with diverse types of secreted structures whose

form and arrangement is species specific. These secretions include calcareous spicules, spines, and scales, and

chitinous hairs (Fischer-Piette and Franc, 1960) (Figs. 1, 2). The dorsal surface can produce several types of

hard parts, while the mantle edge and ventral surfaces generally produce one type of ornament each (Hyman,

1967). These structures can be completely or partially embedded in the cuticle that covers the epidermal cells of

the girdle. These girdle formations, or ornaments, can be simple or composite structures (Fig. 1). Individual,

fusiform, calcareous spicules are often totally embedded in the cuticle, which is 25 to 100µm thick, whereas

longer calcareous spines (Figs. 1, 2b) have only their proximal ends in the cuticular matrix (Plate, 1898, 1902;

Hyman, 1967). Many species produce overlapping calcareous scales (Fig. 2a) that are also connected to the

cuticle basally. Species in several families produce hairs (Fig. 2c), often called setae or bristles, that can be

simple, jointed (articulated), or composite chitinous shafts that extend beyond the girdle surface. Hairs usually

consist of an extension of the cuticular matrix and can be surrounded by a more densely staining cortex (Leise

and Cloney, 1982).

Most spicules are surrounded by a layer or "cup" of material that is darker than the enveloping cuticular matrix

and stains more densely in sectioned material (Figs. 1, 3) (Plate, 1898, 1902; Knorre, 1925; Leise and Cloney,

1982). In spicules from many species, this dense cup is elongated into a shaft that extends from the spicule to

the epidermal cells (Fig. 1). The similarity of many hairs to this type of spicule shaft and the presence of a

spicule at the distal tip of many hairs, led Thiele (1929) and Hyman (1967) to suggest that spicules and hairs

represent the two ends of a continuum of girdle structures. They regard hairs as highly modified shafts of

spicules. I continue their usage here and refer to hairs as those structures in which a chitinous shaft projects

above the surface of the girdle and is the predominant part of the organ.

As will be described below, most hairs contain or are in contact with dendrites from presumptive sensory

neurons. This paper reviews the morphology of chiton hairs while focusing on their neuronal elements and

describes the relationships of these hairs to other girdle ornaments.

DIVERSE GIRDLE HAIRS: AN OVERVIEW

Hairs occur in a bewildering range of sizes and configurations in species from at least five families: Chitonidae;

Lepidochitonidae (Ferreira, 1982); Callochitonidae; Chaetopleuridae; and Mopaliidae [classification after

Bergenhayn (1955) unless otherwise cited]. In addition, hairs from many species of chitons will erode during

the animal's lifetime. Thus' it can be difficult to understand the morphology of a particular type of hair if only

large hairs or hairs from old animals are studied. Species such as Chiton olivaceus Spengler, 1797 (family

Chitonidae) can produce small marginal hairs 80 to 100μm long (Plate, 1902). In the Lepidochitonidae

(Ferreira, 1982) species such as Tonicella insignis Reeve, 1847 produce small, simple hairs only 100µm long

(Leise, 1983), while others, such as Dendrochiton lirulatus Berry, 1963, produce tufts of hairs up to 500µm

long. Hairs from species of Callochitonidae, such as Eudoxochiton nobilis Gray, 1843, often have large

articulated shafts about 1.5 mm in length (Leise, 1983). On in. tact animals of E. nobilis, even the distal spicules

can be discerned. Species in the Chaetopleuridae and Mopaliidae also display hairs in a wide range of sizes;

although the Chaetopleuridae characteristically produce hairs (Pilsbry, 1893), some species, like Chaetopleura

lurida (Sowerby, 1832) secrete none. The girdle of this species bears spicules with articulated and simple shafts.

A congener, C. peruviani Lamarck, produces similar spicules whose elongated shafts extend beyond the

cuticular surface and so earn them the designation of hair (Plate, 1902; Fischer-Piette and Franc, 1960) (Fig. 4).

Among the Mopaliidae are also species that produce small, simple hairs, such as those on Katharine tunicata

Wood, 1815 or very large, simple hairs, as are found on Plaxiphora obtecta (Carpenter in Pilsbry, 1893) (Table

1).

Most of the above mentioned hairs conform to the hypothesis of Thiele (1929) and Hyman (1967) that hairs are

elongated spicule shafts. However, the large hairs secreted by species in the genera Mopalia and Placiphorella,

and those secreted by some of the Lepidochitonidae, namely Lepidochitona flectens (Carpenter, 1864), and

species in the genus Dendrochiton Berry, 1911 (Ferreira, 1982), do not conform to Thiele's (1929) and Hyman's

(1967) hypothesis. These latter types of hairs are composite structures, built by the replication of many basic

units. They are not simply enlarged or elongated spicule shafts. In the genus Mopalia, the basic unit construct is

a calcareous spicule and its long chitinous shaft This basic unit is serially repeated along an outgrowth of the

cuticle, and with the exception of the groove along which these spicules lie, the entire organ is surrounded by

one or two distinct layers of dense cortical material (Fig. 5) (Leloup, 1942; Leise and Cloney, 1982). Similarly,

in the genus Placiphorella, the hair is an extension of the cuticle and is entirely covered with spicules that lie in

whorls just below the surface of the hair (Fig. 2c) (Plate, 1902). From Ferreira's (1982) descriptions, the hairs of

L. flectens and the genus Dendrochiton appear likewise to be branched or compound structures and not simply

enlarged spicule shafts.

THE MORPHOLOGY OF HAIRS OF MOPALIA MUSCOSA: A MODEL FOR COMPOSITE

SENSORY HAIRS

A fully-formed hair of Mopelia muscosa is a curved, distally tapered extension of the cuticle that bears a mesial

groove in which lies a row of spicules (Figs. 5, 6). Each spicule occurs atop a distinct shaft, whose proximal end

is embedded in the cuticular matrix, or medulla. The medulla as enveloped by a bilayered cortex, except for the

mesial groove, and is therefore exposed to the environment along the length of that groove. Within the medulla,

the proximal end of each spicule shaft surmounts a bulbous epidermal projection, a stalked nodule (Leise and

Cloney, 1982) or morgensternförmig Körper" (morning star-shaped body) (Reincke, 1868). Blumrich (1891),

Knorre (1925), and Plate (18

98, 1902) described such nodules in many species. All of these authors suggest that

the nodules are tactile. Until recently (Leise and Cloney, 1982), their presence in hairs of the Mopaliidae was

unknown.

The dorsal girdle epidermis is a single layer of cells that is divided into numerous packets or papillae of

columnar cells. These papillae produce the hairs, spicules, and nodules. Smaller cuboidal cells occur

ubiquitously between the papillae. The papillae that produce the hairs are the largest in the epidermis and as a

hair matures, the papilla comes to lie in a small depression or pocket below the level of the rest of the epidermal

cells (Leise and Cloney, 1982; Leise, 1986).

Each subcortical cell produces a bundle of cortical fibers (Figs. 6, 7). The fiber bundles of the inner cortex are

more dense than those of the outer cortex (Leise and Cloney, 1982). Each layer of the cortex in a mature hair is

several bundles thick, whereas in young hairs the cortex is only one bundle wide. Newly forming hairs have no

cortex and start as a single spicule with an elongated shaft that lies above a stalked nodule. More spicules and

their associated shafts and nodules are added to the growing cuticular hair and only after several nodules are

present does cortex begin to appear. The cortex is initially a narrow crescent along the lateral edge of the hair.

As development proceeds, the hair grows longer and the cortex become progressively wider until it

encompasses nearly the entire shaft (Leise, 1986).

Submedullary cells occur as a hillock that protrudes into the base of the hair shaft and presumably secrete the

medullary matrix. The sensory cells lie in clusters within this hillock and each cluster produces a long bundle of

dendrites oat extends through the hair (Figs. 6-9) (Leise and Cloney, 1982). The oldest dendritic bundle extends

to the tip of the hair; younger bundles are progressively shorter. Each dendritic bundle ends in a nodule, just

below the shaft of a mesial spicule (Fig. 6). A hair can have from one to 20 nodules in arising from the same

number of neuronal clusters in the submedullary hillock (Leise and Cloney, 1982). One or several nerves

emerge from the base of each trichogenous (hair-producing) papillae (Figs. 6, 7, 10). These nerves are

preesumed to contain the axons of the submedullary sensory neurons (Fig. 10). Although these basal axons have

not been definitively shown to arise from the neurons (i.e. the submedullary neurons could be axonless,

synapsing upon sensory interneurons from the CNS, or the submedullary 'neurons" could have been

misidentified and the nerves could have other functions) (see also following section), the most obvious

explanation is that the epidermal cells whose long apical necks contain numerous parallel microtubules are

primary sensory neurons (Leise and Cloney, 1982). Finally, there are usually fewer nerves than nodules within

one papilla, indicating that the axons from several clusters of neurons converge onto a single nerve (Fig. 6).

Each nodule (and hence each dendritic bundle) contains dendrites from several cells, there being from one to 25

dendrites per bundle (Fig. 9) (Leise and Cloney, 1982). Each bundle is surrounded by one or two submedullary

supporting cells. The dendrites often branch, so a tally of the number 01 dendrites in a bundle overestimates the

number of sensory neurons. In figure 6 the sensory dendrites are drawn as straight cylinders with only one

neuron per cluster for ease of presentation. Within the nodule, the dendrites ramify between the processes of the

submedullary supporting cells that contain large vacuoles (Fig. 11).

SENSORY HAIRS FROM OTHER MOPALIIDAE

To gain some understanding of the occurrence of sensory hairs throughout the Mopaliidae, I examined the

girdle integuments of six other species in this family. Animals were collected from rocky intertidal regions in

Puget Sound, Washington, or on Vancouver Island, British Columbia (Leise, 1983). Samples of girdle

integuments were fixed in Millonig's phosphate buffered glutaraldehyde and post-fixed in bicarbonate buffered

osmium tetroxide (Cloney and Florey, 1968). Detailed procedures are described elsewhere (see Leise and

Cloney, 1982; Leise, 1983). Specimens of Plaxiphora obtecta were obtained indirectly from New Zealand,

where they were fixed in 5% formalin in seawater.

In addition to various shell and body characteristics, one of the mopaliid diagnostic features is the production of

dorsal girdle hairs. From most accounts, the one exception In this hairy family appeared to be Katharina

tunicata. However, Leloup (1940) noticed that the girdle of this species produces tiny translucent hairs (Table

1). I confirmed this observation and found that the papillae that secrete these hairs are also innervated (Fig. 12).

Three other species of Mopalia, namely M. ciliata, M. hindsii, and M. lignosa, have innervated hairs similar to

those of M. muscosa (Fig. 13). Interspecific variation occurs in size, number of nodules per hair, extent of

cortical envelopment, and size and arrangement of spicule shafts (Leise, 1983).

The hairs of Placiphorella velata Dail 1878 (Fig. 2c) are quite different from those in the genus Mopalia.

Placiphorella hairs contain no nodules, although they are innervated (Plate, 1902; Leise, 1983). Instead of lying

above a nodule, each spicule in these hairs lies above a cell that projects beyond the hillock on a thin stalk (Fig.

14). The ultrastructure of these cells deserves attention as they too are likely to be sensory neurons. As Plate

(1902) reported for P stimpsoni (Gould, 1859), several nerves emerge from the epidermis below each of the

hairs of P velata. Again, these nerves probably carry axons from the primary sensory neurons, and axons from

many neurons converge into each nerve.

I also examined the hairs of Plaxiphora obtecta, which are large discrete shafts of cortical material (Fig. 15,

Table 1). In sectioned material I found no nerves emerging from the bases of their trichogenous papillae. With

this exception, all of the mopaliid hairs that I examined either contained or contacted epidermal neurons (Leise

and Cloney, 1982; Leise, 1983). The hairs of P obtecta could truly lack innervation, or this lack could be the

result of inadequate fixation.

Stalked nodules, such as those in hairs of mopaliid genera, have been observed in the epidermis of many chitons

(Fig. 3; Table 2) and repeatedly hypothesized to be tactile (Blumrich, 1891; Plate, 1898, 1902; Knorre, 1925;

Thiele, 1929; Haas and Kriesten, 1975; Fischer et al., 1980). However, the papillae that produce these nodules

had not been shown to send nerves into the dermis until the work of Leise and Cloney (1982; Leise, 1983). All

stalked nodules are not identical, as is discussed below. The functional distinctions between the various types of

nodules are unknown.

OCCURRENCE OF SENSORY NODULES IN THE CHITONS

According to Blumrich (1891), all chitons possess a fringe of spicules around the mantle edge. In many cases,

the shafts of these marginal spicules contain or surmount a stalked nodule (Table 2) (Plate, 1898, 1902; Knorre,

1925). The hollow shafts of spicules in some species contain more claviform (club-shaped) cellular protrusions

that lack a slender stalk (Blumrich, 1891; Plate, 1898, 1902; Knorre, 1925). I examined the ultrastructure of

claviform nodules in Katharina tunicata and found that they too contain dendrites from epidermal sensory

neurons and that the dendrites ramify between vacuolated processes of epidermal supporting cells. Other

epidermal protruberances described by Fischer et al. (1980) resemble incipient stalked nodules of Mopalia

muscosa (Leise, 1983). In this review I refer to all of these epidermal protrusions as stalked nodules.

Only on the dorsal surface of the girdle are stalked nodules reported to occur alone (Fig. 3) (Blumrich, 1891;

Haas and Kriesten, 1975; Fischer et al., 1980; Leise and Cloney, 1982; Leise, 1986). In most cases, dorsal

nodules are subjacent to spicules. The ventral girdle in all chitons produces overlapping spicules (Blumrich,

1891; Pilsbry, 1892, 1893; Knorre, 1925; Fischer-Piette and Franc, 1960; Hyman, 1967) and in many cases

these spicules also contact sensory nodules (Table 2). Two exceptions are Placiphorella veleta and stimpsoni, in

which the ventral spicules contact stalked cells That are much like those in the dorsal hairs. These cells too will

probably prove to be sensory neurons upon further study. Curiously, in P veleta the marginal spicules are

associated with typical stalked nodules (Plate, 1902; Leise, 1983).

Of the chitons I studied, in only two species did I find claviform nodules without innervated papillae:

Eudoxochiton nobilis and Plaxiphora obtecta. These animals were fixed in 5% formalin (see Leise, 1983)

which does not preserve cellular ulrastructure as well as the combination of glutaraldehyde and osmium

tetroxide. Thus, it is possible that the slender 1-2µm in diameter) epidermal nerves were not preserved well

enough for me to recognize them. It would be most surprising if these two species alone show no innervated

epidermal sensory organs.

FUNCTIONS OF CHITON HAIRS

The functions of chiton hairs are not well understood although plausible hypotheses abound. Hyman (1967)

describes chiton hairs as armature, although chitons bearing hairs are successfully preyed upon by starfish

(Mauzey et al., 1968; Paine, 1980), seagulls (Moore, 1975), fish (Ronald Shimek, pers. comm.) and humans.

The girdle could be toxic distasteful but it does not provide sufficient protection against predation. Predators

tend to eat the foot and viscera, discarding the shell and girdle.

Species with large and abundant hairs such as Mopalia muscosa often support extensive epiphytic and epifaunal

communities (Phillips, 1972). This covering retains water and could protect the animal against desiccation at

low tides. This covering could also provide an additional defense against predation. Pisaster ochraceus (Brandt,

1835) will feed on M. muscosa, but if the chiton is covered with its normal detrital cloak, the starfish may fail to

recognize it. After it touches an overgrown chiton, a starfish will ignore it. The basis for this protection, that is,

whether the starfish's olfactory or tactile senses are deceived, is unknown. If the starfish contacts the girdle of a

clean chiton, it detects a prey item and removes the chiton from the substratum. A chiton cannot escape a

hungry starfish nor maintain a sufficiently strong grip on the substratum to avoid being consumed (pers. obs.).

A chiton's epiphytic cloak could also afford protection from visual predators. Chitons with well developed

epiphytic communities often resemble clumps of algae. Even during high tides, while they are moving and

feeding, their identity could be concealed, as their slow rate of motion does not reveal their animal nature.

In addition to providing passive defenses, chiton hairs also mediate active responses from the animal. Chitons

whose hairs are bent or pinched will turn away from the source of stimulation, or after several stimuli, tighten

their grip on the substratum and remain motionless. This response appears to habituate rapidly, as prolonged or

repeated stimulation will soon fail to invoke a response (Leise, 1983).

This tactile aspect of hair function could be most important to juveniles. In Mopalis muscosa, hairs first appear

at metamorphosis (Leise, 1984) and although they do not initially display all of the adult characteristics, the first

sensor/ neurons have differentiated and are presumably operational (Leise, 1986). These young animals take

refuge in cracks and crevices in the substratum and their hairs may be important detectors of irregular surface

features. Similarly, ventral nodules, which are widespread among the chitons, would give an animal feedback

on the surface characteristics of its substratum and allow it to modulate its grip.

Although chiton hairs respond to touch, mechanoreception may not be their primary function. For example, they

could be chemoreceptive. However, unlike other molluscan chemoreceptors (Laverack, 1968), the dendrites in

the stalled nodules are embedded in the cuticle. I found no pores in the cuticle as exist in insect chemoreceptive

hairs (Laverack, 1968). I was also unable to elicit any response from Mopalis muscosa upon application to the

hairs (without moving the hairs) of various algae or tube feet from a predator starfish Pisaster ochraceus.

As previously stated, a sensory function is the most parsimonious explanation for the presence of an innervated

integument and cells that resemble sensory neurons. However, this explanation does not exclude the possibility

that the basal nerves mediate other functions, such as contraction or secretion. I found no obvious contractile

elements in the epidermis of Mopalis muscosa, although its skin does secrete the cuticle and ornaments.

Epidermal cells in other species such as Katharina tunicata extrude pigment granules into the cuticle (Fig. 12)

(Leise, 1983). Whether or not the nerves carry axons from neurons mediating epidermal secretion is unknown.

CONCLUSIONS

My results lead me to suggest that most chiton hairs are mechanoreceptors, although hairs are not the only

girdle sensory organ. Stalked nodules occur far more widely than hairs, on the marginal and ventral surfaces of

what may be a majority of the chitons (Table 2). These nodules are probably important sources of feedback to

the animal about the nature of the surface on which it lives. Fischer et al. (1980) have also recognized

photoreceptors in the girdle of Acanthochiton fascicularis that could in part be responsible for this chiton's

response to changes in light intensity. Unfortunately, the existence of these girdle sensory organs is not widely

recognized.

In her review of the functional morphology of the chiton epidermis, Hyman (1967) did not assimilate Plate's

(1902) information about the sensory nature of girdle hairs nor the sentiment from the German literature that

stalked nodules are tactile (Blumrich, 1891; Plate, 1898; Knorre, 1925; Thiele, 1929). Since then, the sensory

nature of girdle structures has been studied or remarked upon by several authors (Beedham and Trueman, 1967;

Haas and Kriesten, 1975; Fischer et al., 1980). Most invertebrate texts include descriptions of chiton sensory

organs in the mouth, on the subradular organ, in the buccal cavity, in the pallial grooves, and in the shell plates,

but not in the girdle (Hyman, 1967; Meglitch, 1971; Gardiner, 1972; Barnes, 1987; Pearse et al., 1987).

In Mopalia muscosa, hairs erode and lose spicules throughout the animals's life. As many species produce hairs

and do so constantly during their lifetimes, the benefits from their presence must outweigh their productive

costs. Hairs appear to have evolved several times in this class, as large hairs occur in diverse families and can be

formed in several ways. Evolutionarily, there appear to be trends towards an increase in the size of girdle

ornaments (Pilsbry, 1892; Leise, 1983) and towards an inclusion of sensory organs in these ornaments. Hairs

are thus considered to be phytogenetically advanced features, as they also occur in stratigraphically newer

families (Smith, 1960) and appear late in an animal's development.

The integument of most molluscs is richly endowed with sensory organs and individual sensory neurons that

serve many modalities, including mechanoreception, chemoreception, and photoreception (Laverack, 1968). For

the chitons to be "blind" to environmental stimuli over a large portion of their skin would indeed be surprising

(Beedham and Trueman, 1967). The work of many authors reviewed here suggests that this is certainly not the

case and that the girdle ornaments are not just passive armature but active participants in the lives of these

animals.

LITERATURE CITED

Barnes, R. D. 1987. Invertebrate Zoology Saunders College, Philadelphia, Pennsylvania. pp. 395-400.

Beedham, G. E. and E. R. Trueman. 1967. The relationship of the mantle and shell of the Polyplacophora in

comparison with that of other Mollusca. Journal of Zoology, London 151:215a,

Bergenhayn, J. R. M. 1955. Die fossilen schwedischen Loricaten netts einer vorlufigen Revision des Systems

der ganzen Klass, Loricata. Acta Universitets Lundensis 2, NS 51(8)1-14.

Blumrich, J. 1891. Das integument der Chitonen. Zeitschrift lur Wissenschaftliche Zoologie 52(3):404-476.

Cloney, R. A. and E. Florey. 1968. The ultrastructure of cephalopod chromatophore organs. Zeitschrift fiir

Zellforschung 89:250-281

Ferreira, A. J. 1982. The family Lepidochitonidae Iredale, 1914 (Mollusca: Polyplacophora) in the Northeastern

Pacific. Vette 25(2):93-138.

Fischer, F. R, W. Maile and M. Renner. 1980. Die Mantelpapillenund Stacheln von Acanthochiton fascicularis

L. (Motion Polyplacophora). Zoomorphology 94:121-131.

Fischer-Piette, E. and A. Franc. 1960. Classe des Polyplacophores, In: Traitd de Zoologie. Anatomie,

Systematique, Biologie 5121 P.- P. Grasse, ed. pp. 1701-1785. Masson et Cie, Paris.

Gardiner, M. S. 1972. The Biology of Invertebrates McGraw-Hill BO Co., New York, New York. pp. 637, 677.

Haas, W. and K. Kriesten. 1975. Studien uber das Perinotum-Epithe und die Bildung der Kalkstacheln von

Lepidochitona cinerel (L.) (Placophora). Biomineralisation 8:92-107.

Hyman, L. H. 1967. The Invertebrates VI. Mollusca I. McGraw-Hill Bed Co., New York, New York. pp. 74-82.

Knorre, H. von. 1925. Die Schale und die RUckensinnesorganewe Trachydermon (Chiton) cinereus L. und die

ceylonischechitone der Sammlung Plate. Jenaische Zeitschrift fiir Naturwasat schaftlichen Medizinische

61(54):469-632.

Laverack, M. S. 1968. On the receptors of marine invertebrates. Oceanography and Marine Biology Annual

Review 6:249-324

Leise, E. M. 1983 Chiton integument: Ultrastructure and development of sensory ornaments. Doctoral

Dissertation, University of Washington, Seattle, Washington. pp. 1-196.

Leise, E. M. 1984. Chiton integument: Metamorphic changes in Mopalia muscosa (Mollusca, Polyplacophora).

Zoomorphology 104:337-343

Leise, E. M. 1986. Chiton integument: Development of sensory organs in juvenile Mopalia muscosa. Journal of

Morphology 189

Leise, E. M. and R. A. Cloney. 1982. Chiton integument: Ultrastructure of the sensory hairs of Mopalia

muscosa (Mollusca: Polyplacophora). Cell and Tissue Research 223:43-59.

Loup, E. 1940. Caracteres anatomique de certains Chitons de la cote californienne. Bruxelles Me'moires du

Muscle Royal D'Histoire Naturelle de Belgique 17:2-41. Leloup, E. 1942. Contribution a la connaissance des Polyplacophores. I. Famille Mopaliidae, Pilsbry, 1892.

Bruxelles Mdmoires du Muscle Royal D'Histoire Naturelle de Belgique 25:2-63.

Mauzey, K. P., C. Kirland and P. K. Dayton. 1968. Feeding behavior of asteriods and escape responses of their

prey in the Puget Sound region. Ecology 49(4):603-619.

Meglitsch, P. A. 1971. Invertebrate Zoology. Oxford Press, New York, New York. pp. 291-196.

Moore, M. 1975. Foraging of the western gull Larus occidentalis and its impact on the chiton Nuttallina

californica. Veliger 18 (suppl):51-53.

Paine, R. T. 1980. Food webs: Linkage, interaction strength and community infrastructure. Journal of Animal

Ecology 49:667-685. Pearse, V., J. Pearse, M. Buchsbaum and R. Buchsbaum. 1987. Living Invertebrates.

Blackwell Scientific Publications, Palo Alto, California. pp. 319-325.

Phillips, T. 1972. Mopalia muscosa Gould (1884) as host to an intertidal community. Tabulata 5(1):21-23.

Pilsbry, H. A. 1892. Polyplacophora. In: Manual of Conchology Vol. 14 G. W. Tryon, ed. pp. 1-350. Academy

of Natural Sciences, Philadelphia, Pennsylvania.

Pilsbry, H. A. 1893. Polyplacophora. In: Manual of Conchology Vol. 14 G. W. Tryon, ed. pp. 1-133 Academy

of Natural Sciences, Philadelphia, Pennsylvania.

Plate, L. H. 1898. Die Anatomie und Phylogenie der Chitonen. Teil A. Zoologische Jahrbiicher; Suppl. 4:1-

241.

Plate, L. H. 1902. Die Anatomie und Phylogenie der Chitonen. Teil. B, C. Zoologische Jahrbiicher, Suppl.

5:15-216, 281-600.

Reincke, J. 1868. Beitrage zur Bildungsgeschichte der Stacheln im Mantelrande der Chitonen. Zeitschrift kir

Wissenschaftlische Zoologie 13:305-321.

Smith, A. G. 1960. Amphineura. In: Treatise on Invertebrate Paleontology. R. C. Moore, ed. pp. 141-176.

University of Kansas Press, Lawrence, Kansas.

Thiele, J. 1929. Erste Klasse des Stammes der Mollusca, Loricata. In: Handbuch der systematischen

Weichtierkunde 5(1), W. Kiikenthal and T. Krumbach, eds. pp. 1-22. A. Asher and Co., Amsterdam.

Date of manuscript acceptance: 13 November 1987